Aquatic Invasions (2010) Volume 5, Issue 1: 97-102
This is an Open Access article; doi: 10.3391/ai.2010.5.1.11
© 2010 The Author(s). Journal compilation © 2010 REABIC
Proceedings of the 16th International Conference on Aquatic Invasive Species (19-23 April 2009, Montreal, Canada)
Research article
Experimental evaluation of the impacts of the invasive catfish Hoplosternum
littorale (Hancock, 1828) on aquatic macroinvertebrates
Craig Duxbury1* , Jeff Holland 2 and Marianne Pluchino 3
1
Walt Disney Imagineering, Research and Development, 1365 Ave. of The Stars, Lake Buena Vista, Florida, USA
Reedy Creek Improvement District, 2191 South Service Ln., Lake Buena Vista, Florida, USA
3
Seminole County, Surface Water Quality, 1101 East First St., Sanford, FL, 32711, USA
E-mail: [email protected] (CD), [email protected] (JH), [email protected] (MP)
2
*
Corresponding author
Received: 28 August 2009 / Accepted: 16 February 2010 / Published online: 22 February 2010
Abstract
The hoplo catfish [Hoplosternum littorale (Hancock, 1828)] is a callichthyid catfish native to South America. It was first
recorded in Florida in 1995. It has now dispersed throughout much of Florida. It is thought that this fish has had little or no
impacts to native fish. However, it is unknown if the introduction of this fish can cause other ecol ogical impacts, such as
alteration of aquatic invertebrates assemblages. We conducted a cage experiment to evaluate the effects of the hoplo catfish on
macroinvertebrates. Results showed that macroinvertebrate abundance and taxa on artificial substrates (MAS) were reduced by
31 and 50% in the fish treatments, respectively. The entire macroinvertebrate assemblage structure was significantly different
between fish and no-fish treatments. This difference was driven primarily by reductions in amphipods, and chironomids.
Macroinvertebrates were also identified from fish stomachs and these were compared to assemblages on the MAS. We found a
smaller subset of taxa in the stomachs, as compared to the MAS. These results suggest that this fish could alter the
macroinvertebrate assemblage structure. This could have implications for environmental monitoring programs that use
macroinvertebrates to assess water quality.
Key words: aquatic invasive species, cage experiments, biomonitoring, Florida
Introduction
Invasive species are considered to be a
significant threat to biodiversity (Levine 2008).
Non-native, invasive fish have also contributed
to the worldwide loss of biodiversity (Clavero
and Garcia-Berthou 2005). Introduced and
invasive fishes are now present in all states and
all major aquatic ecosystems in the United
States. A moderate climate, extensive waterbodies, and a large human population means that
Florida has 127 nonindigenous fish species
(Fuller et al. 1999). In 1995, the hoplo catfish
[Hoplosternum littorale (Hancock, 1828)], a
callichthyid catfish native to South America, was
reported in Florida (Nico et al. 1996), and has
rapidly spread throughout the state (Fuller et al.
1999; Pearlstine et al. 2007; Gestring et al. 2009;
Emerson 2007). This fish exhibits a number of
characteristics typical of successful invaders,
including tolerance to a wide range in
temperature and dissolved oxygen (Brauner et al.
1995), a wide dietary breadth (Mol 1995), and
high fecundity (Hostache and Mol 1998; Nico
and Muench 2004).
Many experimental and observational studies
have shown that fish can have significant topdown and bottom-up impacts on primary and
secondary production (Matsuzaki et al. 2008).
Furthermore, introductions of fish can lead to
ecological cascades (Kaufman 1992) and
alteration of nutrient cycles (Schindler et al.
2001), and changes in aquatic (Power 1990) and
terrestrial food webs (Baxter et al. 2004). Fish
predation has been found to be a strong influence
on the structure of macroinvertebrate assemblages (Williams and Taylor 2003; Cheever and
Simon 2008; Flecker 1992a; Allan 1982;
Dudgeon 1991; Miller and Crowl 2005). In
addition, introduced fish can also impact
macroinvertebrate assemblages (Flecker and
Townsend 1994; Knapp et al. 2001); however,
this result is not always certain (Harig and Bain
1998; Englund and Polhemus 2001).
Macroinvertebrates are a diverse group of
organisms, that are important component of
freshwater ecosystems (Wallace and Webster
1996). Because of their high abundance and a
wide range in environmental tolerances, these
organisms are frequently used in biomonitoring
97
C. Duxbury et al.
programs to assess water quality (Rosenberg and
Resh 1993). In these programs, changes in
macroinvertebrate assemblages are assumed to
be due to changes in water quality. However,
biotic interactions are not often assessed,
especially for a novel invader. Thus, our
objective was to assess the effects of this fish on
the macroinvertebrate assemblage of central
Florida.
Materials and methods
The study site was located on Reedy Creek, a
blackwater stream (Meyer 1990) in the
Kissimmee River watershed. The stream is
characterized by relatively low nutrients, low
ionic strength, and high concentrations of
organic acids (Hampson 1993). This lowgradient stream flows through extensive, mixed
hardwood swamps, dominated by cypress
[Taxodium distichum (L.) L.C. Rich.].
We used enclosure cages (n = 10) to test the
effects of fish on macroinvertebrates. The experimental design included two treatments: fish and
a control with no fish, with five replicates per
treatment. Cages were 1m (H) × 0.82m (L)× 0.65m
(W) composed of polyvinyl pipes forming the
frame and then completely covered with 14 mm
mesh size aquaculture screen. Cages were
secured to the stream bottom with metal stakes.
Cages were placed in pairs, the two located next
to each other in areas of similar depth and
velocity; one cage with fish, and the control
treatment. Water depth in cages ranged from
0.52 to 0.88 m. Water velocity averaged 0.4 and
0.2m sec-1 outside and inside the cages, respectively. Debris was cleared from the front of the
cages once per week.
Prior to the start of the experiment (October
2005), we caught the hoplo catfish from the
study stream using a cast net. We then placed
two catfish into each fish-treatment cage. We
chose two fish per cage for several reasons. The
first is that there are no published reports of
typical brown hoplo densities. Second, it appears
that these fish exhibit schooling behavior based
on our observations (unpublished data) and
synchronized breathing behavior has been
reported (Sloman et al. 2009). The ten fish
averaged 205 mm (range: 176 to 246 mm) in
total length, and 159 g in average weight (range:
113 to 227 g).
98
Macroinvertebrate analyses
Stream invertebrates were quantified using a
modification of the 14 plate artificial substrates
(APHA et al. 1989), hereafter referred to as
macroinvertebrate artificial substrates (MAS).
We modified the MAS by reducing the number
of hardboard plates from 14 to five per artificial
substrate. Three MAS were placed in each
treatment cage, attached with monofilament line
in the center of the cage. After 28 days, the MAS
and fish were removed from the cages. At the
laboratory, the MAS were disassembled, and the
macroinvertebrates were carefully dislodged
using soft brushes. Macroinvertebrates were
sorted alive. The macroinvertebrates were then
identified to the family or order. The total
number of individuals and total number of taxa
were calculated separately for each MAS. Since
cages were the experimental units, we averaged
the numbers of individuals and taxa from the
three MAS for each cage to obtain a mean
number per cage.
Stomach analyses
At the end of the experiment, fish were
sacrificed, weight and length were measured, and
stomachs were removed. The macroinvertebrate
data were pooled from the two fish in each cage.
Invertebrates in the stomachs were identified and
enumerated to the lowest practicable level, as
noted above.
Water quality
At the beginning and end of the experiment
temperature, conductivity, dissolved oxygen, and
pH was measured with a Hydrolab Quanta meter.
Measurements were made mid-depth, approximately 0.25 m.
Analyses
Differences
in
macroinvertebrates
(total
individuals and taxa) between fish and no-fish
treatments were compared with t-tests after
checking for homogeneity of variances. Since we
found no evidence of heterokedasticity, we used
the untransformed data. The relationship
between fish length and number of organisms
found in the stomachs were assessed using
simple linear regression. Univariate statistics
were calculated with Statistica Ver. 7.1 (StatSoft
2006).
Impacts of Hoplosternum littorale on aquatic macroinvertebrates
We also conducted several multivariate
analyses to examine the impacts of fish on
macroinvertebrates. First, we used nonmetric
multidimensional scaling (MDS) to visualize
patterns in the entire macroinvertebrate assemblage structure between fish and no-fish MAS
(Clarke 1993; Clarke and Ainsworth 1993). This
nonparametric technique was based on the BrayCurtis similarity matrix of the fourth-root
transformed macroinvertebrate assemblage data.
Organisms were averaged from the three MAS
per cage for this analyses. A 4 th root transformation was applied to downweight the strong
dominance from several taxa. An analyses of
similarity (ANOSIM) was then used to test for
significant differences between the treatments.
ANOSIM is a nonparametric permutation
procedure applied to the rank similarity matrix
underlying the MDS ordination that compares
the degree of differences among treatment
groups, and calculates an R statistic. The significance level of the R statistic is calculated by
comparing to a permutation distribution (Clarke
1999). We used 9,999 permutations on the BrayCurtis distance of the 4th root transformed data.
SIMPER was used to calculate the contributions
of each taxon to differences. The multivariate
analyses were conducted using the PRIMER-E
software package 6.1.11 (Clarke and Warwick
2001).
Results
Water quality
Temperature and dissolved oxygen decreased
from the beginning to the end of the experiment
(Table 1). Conductivity and pH did not change
between the time periods.
Macroinvertebrates
A total of 1,998 macroinvertebrates were
identified from the MAS. On average, there were
about 30% fewer organisms found on the MAS
in the fish treatments (p = 0.08, 2 sided t-test)
(Figure 1A). There were a total of 11 taxa, and a
50% reduction in taxa richness on the fish
treatment MAS (Figure 1B) (p=0.05). Chironomids and oligochaetes dominated, accounting for
greater than 90% of the total number of
organisms. Chironomids comprised 46 and 63%,
and Oligochaeta comprised about 50 and 31%, of
the organisms on the MAS in the fish and no-fish
treatments, respectively.
Table 1. Physiochemical water quality data in stream at start
and end of experiment, measured with a hand-held meter.
Value at
Beginning of
Experiment
Value at End
of Experiment
Temperature (ºC)
25.1
18.5
Dissolved Oxygen
(mg/L)
3.9
0.96
Conductivity (µS/cm)
139
139
pH
6.2
6.2
Parameter
Table 2. A comparison of the relative abundance (within
treatments) of taxa (Family or Order level) found on the
artificial substrates (MAS) in fish and no-fish treatments
(n=10, each), and in the stomach contents of caged fish
(n=10).
Family or Order
Fish
MAS
No Fish
MAS
Caged Fish
Stomach
Chironomidae
46.3
63.2
87.9
Oligochaeta
50.3
30.6
0.0
Gastropoda
2.30
4.00
1.7
Amphipoda
0.13
0.80
5.5
Odonata
0.63
0.50
0.0
Ephemeroptera
0.00
0.10
0.0
Clitellata
0.00
0.10
0.0
Collembola
0.38
0.08
0.0
Coleoptera
0.00
0.10
0.0
Acarifomres
0.00
0.00
1.7
Bivalva
0.00
0.20
1.0
Decapoda
0.00
0.00
0.3
Ceratopogonidae
0.13
0.33
1.7
Table 3. Results from SIMPER analyses indicating the five
dominant taxa that contributed the greatest influence in
differences in macroinvertebrate assemblage structure
between fish and no-fish MAS. Average abundance based on
4th root transformed data.
Average
Abundance
Fish
Treatment
0.15
Average
Abundance
No-Fish
Treatment
0.73
Odonata
0.50
0.40
13.3
Chironomidae
2.20
2.64
12.3
Ceratopogonidae
0.15
0.48
11.8
Oligochaeta
2.24
2.14
9.7
Taxa
Amphipoda
Contribution (%)
17.1
99
C. Duxbury et al.
Stomach analyses
A total of 290 organisms were identified from
the fish stomachs collected from the caged fish.
There were nine to 65 organisms per stomach
There was no relationship between length of fish
and the number of organisms found in the
stomachs (p>0.05). Seven taxa were found in the
stomachs of the caged fish (Table 2).
Chironomids were the most abundant taxa,
accounting for almost 90% of the total number of
organisms found in the stomachs of the caged
fish. Amphipods were the second most abundant
taxon, accounting for almost 6% of the total
number of organisms.
Multivariate analyses
The MDS plot shows a clear separation in
macroinvertebrate assemblages between fish and
no-fish treatments (Figure 2). The relatively low
stress (0.14) indicates that these data can be
effectively described in two-dimensional space
(Clarke and Warwick 2001). The ANOSIM test
showed that there were significant (R=0.424, P =
0.032)
differences
in
macroinvertebrate
assemblages between treatments. The SIMPER
analyses indicated that the difference in
assemblage structure was influenced by five taxa
which accounted for a cumulative contribution of
64% (Table 3). The difference in assemblage
structure was primarily influenced by larger
numbers of dragonflies (Odonata) and fewer
numbers of amphipods, chironomids, and the
biting chironomids (Ceratopogonidae) on the fish
treatment MAS.
Figure 1. (A) Mean (+/-1 SE) number of organisms collected
from the modified artificial substrates (p =0.08). (B) Mean
(+/-1 SE) number of taxa from the MAS (p =0.05). Dark bars
represent fish treatment and hatched bars represent no-fish
treatments.
Discussion
Our results suggest that hoplo catfish impact
aquatic macroinvertebrate assemblages on
artificial substrates. We found that macroinvertebrate abundances and taxa richness on
MAS in cages with fish were significantly
reduced by about 30 and 50%, respectively
(Figures 1A, B). While there are many examples
in the literature documenting strong impacts of
fish on macroinvertebrates in freshwater systems
(Flecker 1992b; Dudgeon 1991; Williams and
Taylor 2003; Englund and Polhemus 2001; Gido
2003; Ruetz et al. 2006; Baxter et al. 2004;
Miller and Crowl 2005) the results are
sometimes equivocal (Allan 1982; Flecker and
Allan 1984; Culp 2009; Reice 1991; Englund and
Polhemus 2001).
100
Figure 2. Nonmetric multidimensional scaling plot (MDS)
showing macroinvertebrate assemblages (MAS) collected
from artificial substrates in cages with fish (▲) and no-fish
(●). Each symbol represents the average of three MAS.
Impacts of Hoplosternum littorale on aquatic macroinvertebrates
We think that direct predation could be one
explanation for the macroinvertebrate reductions
on the fish treatment substrates. We base this
conclusion on the fact that many of the
macroinvertebrates found in fish stomachs were
similar to macroinvertebrates found on MAS.
Further, chironomids were the most abundant
organism found in the stomachs, and these
insects are a common food item for these fish
(Mol 1995; Gestring et al. 2009). However,
indirect influences could also explain the
reduction in invertebrates. For example, we
observed greater numbers of predatory dragonflies on the fish MAS. This may have been
because the catfish may not eat these insects. A
larger number of dragonflies, could have
decreased the overall number of invertebrates.
Another indirect influence may have been related
to behavioral impacts. The cage mesh size did
not preclude macroinvertebrates from leaving the
cages. Therefore, fish may have caused macroinvertebrates to flee from predation, or may have
simply been dislodged from the MAS. The
presence of fish can result in a strong drift
response from aquatic insects (Flecker 1992a).
Regardless of the mechanism, our results
suggest that these catfish can alter the macroinvertebrate assemblage structure (Figure 2).
Other investigators have found that introduced
fish result in changes in macroinvertebrate
assemblages (Englund and Polhemus 2001;
Miller and Crowl 2005). Alterations of the
macroinvertebrate assemblage and changes in
relative abundances, similar to what we observed
can have important implications for water quality
monitoring programs. Many water quality
monitoring programs incorporate biomonitoring
as part of an environmental assessment. Macroinvertebrates are considered to integrate water
quality, and changes in macroinvertebrate
assemblages are largely assumed to be in direct
response to changes in water chemistry. Thus, a
novel, invasive predator such as the hoplo catfish
could alter the macroinvertebrate assemblage,
leading to incorrect conclusions about water
quality.
While our results suggest that this invasive
catfish could impact macroinvertebrates, clearly
there are uncertainties. For example, a mechanistic explanation would help clarify these
impacts. Also, environmentally realistic fish
densities, especially, as compared to native fish,
should be estimated. To our knowledge, there are
no published data on the densities of these fish.
Finally, the impacts of the hoplo must be
compared to native fish. This knowledge would
lead to a better understanding of the ecological
impacts of this invasive fish.
Acknowledgements
We would like to thank the field biologists who participated
in this study. Specifically, Tom Troffer, and Iwona
Staniswoski helped with gathering these data. This work was
supported by WDI Research and Development, as well as
RCID Environmental Services. We thank them for their
support. Two anonymous reviewers provided helpful
comments on this paper.
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